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Impact of palladium nanoparticles (Pd-NPs) on the biology of neutrophils in vitro and on leukocyte attraction in vivo

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Abstract

Recently, palladium nanoparticles (Pd-NPs) have been shown to possess pro-inflammatory activities. Herein, we investigated potential in vitro effects of Pd-NPs (primary size of 1–10 nm) on the biology of neutrophils, key player cells in inflammation. Also, the aim of this study was to evaluate the pro-inflammatory activity of Pd-NPs using the murine air pouch model, a model previously proposed to be used as a standard assay for testing in vivo pro-inflammatory effects of NPs. Although the positive controls used in vitro give the expected results in all biological functions tested, Pd-NPs do not affect the production of reactive oxygen species and that of interleukin-1β (IL-1β), IL-6, and IL-8. Pd-NPs moderately increase cellular adhesion of neutrophils onto human endothelial cells and significantly increase the capacity of neutrophils to migrate and to delay apoptosis. We conclude that Pd-NPs possess some pro-inflammatory activity in vitro but do not attract leukocytes in vivo regardless of sex.

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References

  • Abrikossova N, Skoglund C, Ahren M, Bengtsson T, Uvdal K (2012) Effects of gadolinium oxide nanoparticles on the oxidative burst from human neutrophil granulocytes. Nanotechnology 23:0957

    Google Scholar 

  • Alarifi S, Ali D, Alkahtani S, Almeer RS (2017) ROS-mediated apoptosis and genotoxicity induced by palladium nanoparticles in human skin malignant melanoma cells. Oxidative Med Cell Longev 2017:8439098

    Google Scholar 

  • Babin K, Antoine F, Goncalves DM, Girard D (2013) TiO2, CeO2 and ZnO nanoparticles and modulation of the degranulation process in human neutrophils. Toxicol Lett 221:57–63

    CAS  Google Scholar 

  • Babin K, Goncalves DM, Girard D (2015) Nanoparticles enhance the ability of human neutrophils to exert phagocytosis by a Syk-dependent mechanism. Biochim Biophys Acta 1850:2276–2282

    CAS  Google Scholar 

  • Barlow PG, Donaldson K, MacCallum J, Clouter A, Stone V (2005) Serum exposed to nanoparticle carbon black displays increased potential to induce macrophage migration. Toxicol Lett 155:397–401

    CAS  Google Scholar 

  • Boscolo P, Bellante V, Leopold K, Maier M, Di Giampaolo L, Antonucci A, Iavicoli I, Tobia L, Paoletti A, Montalti M, Petrarca C, Qiao N, Sabbioni E, Di Gioacchino M (2010) Effects of palladium nanoparticles on the cytokine release from peripheral blood mononuclear cells of non-atopic women. J Biol Regul Homeost Agents 24:207

    CAS  Google Scholar 

  • Chen H, Dorrigan A, Saad S, Hare DJ, Cortie MB, Valenzuela SM (2013) In vivo study of spherical gold nanoparticles: inflammatory effects and distribution in mice. PLoS One 8:e58208

    CAS  Google Scholar 

  • Chhay P, Murphy-Marion M, Samson Y, Girard D (2018) Activation of human eosinophils with palladium nanoparticles (Pd NPs): importance of the actin cytoskeleton in Pd NPs-induced cellular adhesion. Environ Toxicol Pharmacol 57:95–103

    CAS  Google Scholar 

  • Cho WS, Duffin R, Poland CA, Duschl A, Oostingh GJ, Macnee W, Bradley M, Megson IL, Donaldson K (2012) Differential pro-inflammatory effects of metal oxide nanoparticles and their soluble ions in vitro and in vivo; zinc and copper nanoparticles, but not their ions, recruit eosinophils to the lungs. Nanotoxicology 6:22–35

    CAS  Google Scholar 

  • Dahlgren C, Karlsson A, Bylund J (2019) Intracellular neutrophil oxidants: from laboratory curiosity to clinical reality. J Immunol 202:3127–3134

    CAS  Google Scholar 

  • Dianzani C, Cavalli R, Zara GP, Gallicchio M, Lombardi G, Gasco MR, Panzanelli P, Fantozzi R (2006) Cholesteryl butyrate solid lipid nanoparticles inhibit adhesion of human neutrophils to endothelial cells. Br J Pharmacol 148:648–656

    CAS  Google Scholar 

  • Dobrovolskaia MA, McNeil SE (2007) Immunological properties of engineered nanomaterials. Nat Nanotechnol 2:469–478

    CAS  Google Scholar 

  • Durocher I, Girard D (2016) In vivo proinflammatory activity of generations 0-3 (G0-G3) polyamidoamine (PAMAM) nanoparticles. Inflamm Res 65:745–755

    CAS  Google Scholar 

  • Durocher I, Noel C, Lavastre V, Girard D (2017) Evaluation of the in vitro and in vivo proinflammatory activities of gold (+) and gold (−) nanoparticles. Inflamm Res 66:981–992

    CAS  Google Scholar 

  • Girard D (2014) Using the air pouch model for assessing in vivo inflammatory activity of nanoparticles. Int J Nanomedicine 9:1105

    Google Scholar 

  • Goncalves DM, Girard D (2011) Titanium dioxide (TiO(2)) nanoparticles induce neutrophil influx and local production of several pro-inflammatory mediators in vivo. Int Immunopharmacol 21:21

    Google Scholar 

  • Goncalves DM, Girard D (2013) Evidence that polyhydroxylated C60 fullerenes (fullerenols) amplify the effect of lipopolysaccharides to induce rapid leukocyte infiltration in vivo. Chem Res Toxicol 26:1884–1892

    CAS  Google Scholar 

  • Goncalves DM, Girard D (2014) Zinc oxide nanoparticles delay human neutrophil apoptosis by a de novo protein synthesis-dependent and reactive oxygen species-independent mechanism. Toxicol in Vitro 28:926–931

    CAS  Google Scholar 

  • Goncalves DM, Chiasson S, Girard D (2010) Activation of human neutrophils by titanium dioxide (TiO2) nanoparticles. Toxicol in Vitro 24:1002–1008

    CAS  Google Scholar 

  • Gurunathan S, Kim E, Han JW, Park JH, Kim JH (2015) Green chemistry approach for synthesis of effective anticancer palladium nanoparticles. Molecules 20:22476–22498

    CAS  Google Scholar 

  • Hildebrand H, Kuhnel D, Potthoff A, Mackenzie K, Springer A, Schirmer K (2010) Evaluating the cytotoxicity of palladium/magnetite nano-catalysts intended for wastewater treatment. Environ Pollut 158:65–73

    CAS  Google Scholar 

  • Iavicoli I, Farina M, Fontana L, Lucchetti D, Leso V, Fanali C, Cufino V, Boninsegna A, Leopold K, Schindl R, Brucker D, Sgambato A (2017) In vitro evaluation of the potential toxic effects of palladium nanoparticles on fibroblasts and lung epithelial cells. Toxicol in Vitro 42:191–199

    CAS  Google Scholar 

  • Jaillon S, Berthenet K, Garlanda C (2019) Sexual dimorphism in innate immunity. Clin Rev Allergy Immunol 56:308–321

    CAS  Google Scholar 

  • Johansson A, Jesaitis AJ, Lundqvist H, Magnusson KE, Sjolin C, Karlsson A, Dahlgren C (1995) Different subcellular localization of cytochrome b and the dormant NADPH-oxidase in neutrophils and macrophages: effect on the production of reactive oxygen species during phagocytosis. Cell Immunol 161:61–71

    CAS  Google Scholar 

  • Klein SL, Flanagan KL (2016) Sex differences in immune responses. Nat Rev Immunol 16:626–638

    CAS  Google Scholar 

  • Lavastre V, Pelletier M, Saller R, Hostanska K, Girard D (2002) Mechanisms involved in spontaneous and Viscum album agglutinin-I-induced human neutrophil apoptosis: Viscum album agglutinin-I accelerates the loss of antiapoptotic Mcl-1 expression and the degradation of cytoskeletal paxillin and vimentin proteins via caspases. J Immunol 168:1419

    CAS  Google Scholar 

  • Leso V, Iavicoli I (2018) Palladium nanoparticles: toxicological effects and potential implications for occupational risk assessment. Int J Mol Sci 19(2):503. https://doi.org/10.3390/ijms19020503

    Article  CAS  Google Scholar 

  • Leso V, Fontana L, Marinaccio A, Leopold K, Fanali C, Lucchetti D, Sgambato A, Iavicoli I (2018) Palladium nanoparticle effects on endocrine reproductive system of female rats. Hum Exp Toxicol 37:1069–1079

    CAS  Google Scholar 

  • Leso V, Fontana L, Marinaccio A, Leopold K, Fanali C, Lucchetti D, Sgambato A, Iavicoli I (2019) Sub-chronic palladium nanoparticle effects on the endocrine reproductive system of female Wistar rats: preliminary data. Toxicol Ind Health 35:403–409

    CAS  Google Scholar 

  • Liz R, Simard JC, Leonardi LB, Girard D (2015) Silver nanoparticles rapidly induce atypical human neutrophil cell death by a process involving inflammatory caspases and reactive oxygen species and induce neutrophil extracellular traps release upon cell adhesion. Int Immunopharmacol 28:616–625

    CAS  Google Scholar 

  • Lu S, Duffin R, Poland C, Daly P, Murphy F, Drost E, Macnee W, Stone V, Donaldson K (2009) Efficacy of simple short-term in vitro assays for predicting the potential of metal oxide nanoparticles to cause pulmonary inflammation. Environ Health Perspect 117:241–247

    CAS  Google Scholar 

  • Moeller S, Kegler R, Sternberg K, Mundkowski RG (2012) Influence of sirolimus-loaded nanoparticles on physiological functions of native human polymorphonuclear neutrophils. Nanomedicine 8:1293–1300

    CAS  Google Scholar 

  • Murphy-Marion M, Girard D (2018) Titanium dioxide nanoparticles induce human eosinophil adhesion onto endothelial EA.hy926 cells via activation of phosphoinositide 3-kinase/Akt cell signalling pathway. Immunobiology 223(2):162–170. https://doi.org/10.1016/j.imbio.2017.10.030

  • Neubauer N, Palomaeki J, Karisola P, Alenius H, Kasper G (2015) Size-dependent ROS production by palladium and nickel nanoparticles in cellular and acellular environments - an indication for the catalytic nature of their interactions. Nanotoxicology 9:1059–1066

    Google Scholar 

  • Noel C, Simard JC, Girard D (2016) Gold nanoparticles induce apoptosis, endoplasmic reticulum stress events and cleavage of cytoskeletal proteins in human neutrophils. Toxicol in Vitro 31:12–22

    CAS  Google Scholar 

  • Pelletier M, Girard D (2005) Interleukin-15 increases neutrophil adhesion onto human respiratory epithelial A549 cells and attracts neutrophils in vivo. Clin Exp Immunol 141:315–325

    CAS  Google Scholar 

  • Pelletier M, Bouchard A, Girard D (2004) In vivo and in vitro roles of IL-21 in inflammation. J Immunol 173:7521–7530

    CAS  Google Scholar 

  • Petrarca C, Clemente E, Di Giampaolo L, Mariani-Costantini R, Leopold K, Schindl R, Lotti LV, Mangifesta R, Sabbioni E, Niu Q, Bernardini G, Di Gioacchino M (2014) Palladium nanoparticles induce disturbances in cell cycle entry and progression of peripheral blood mononuclear cells: paramount role of ions. J Immunol Res 2014:295092

    Google Scholar 

  • Phan TTV, Huynh TC, Manivasagan P, Mondal S, Oh J (2019) An up-to-date review on biomedical applications of palladium nanoparticles. Nanomaterials (Basel) 10(1):66. https://doi.org/10.3390/nano10010066

  • Poirier M, Simard JC, Antoine F, Girard D (2014) Interaction between silver nanoparticles of 20 nm (AgNP20 ) and human neutrophils: induction of apoptosis and inhibition of de novo protein synthesis by AgNP20 aggregates. J Appl Toxicol 34:404–412

    CAS  Google Scholar 

  • Poirier M, Simard JC, Girard D (2015) Silver nanoparticles of 70 nm and 20 nm affect differently the biology of human neutrophils. J Immunotoxicol 13(3):375-85. https://doi.org/10.3109/1547691X.2015.1106622

    Article  CAS  Google Scholar 

  • Ravindra K, Bencs L, Van Grieken R (2004) Platinum group elements in the environment and their health risk. Sci Total Environ 318:1–43

    CAS  Google Scholar 

  • Reale M, Vianale G, Lotti LV, Mariani-Costantini R, Perconti S, Cristaudo A, Leopold K, Antonucci A, Di Giampaolo L, Iavicoli I, Di Gioacchino M, Boscolo P (2011) Effects of palladium nanoparticles on the cytokine release from peripheral blood mononuclear cells of palladium-sensitized women. J Occup Environ Med 53:1054–1060

    CAS  Google Scholar 

  • Savoie A, Lavastre V, Pelletier M, Hajto T, Hostanska K, Girard D (2000) Activation of human neutrophils by the plant lectin Viscum album agglutinin-I: modulation of de novo protein synthesis and evidence that caspases are involved in induction of apoptosis. J Leukoc Biol 68:845

    CAS  Google Scholar 

  • Schleimer RP, Sterbinsky SA, Kaiser J, Bickel CA, Klunk DA, Tomioka K, Newman W, Luscinskas FW, Gimbrone MA Jr, McIntyre BW et al (1992) IL-4 induces adherence of human eosinophils and basophils but not neutrophils to endothelium. Association with expression of VCAM-1. J Immunol 148:1086

    CAS  Google Scholar 

  • Simard JC, Simon MM, Tessier PA, Girard D (2011) Damage-associated molecular pattern S100A9 increases bactericidal activity of human neutrophils by enhancing phagocytosis. J Immunol 186:3622–3631

    CAS  Google Scholar 

  • Skoczen SL, Potter TM, Dobrovolskaia MA (2011) Method for analysis of nanoparticle effects on cellular chemotaxis. Methods Mol Biol 697:247

    CAS  Google Scholar 

  • Theron AJ, Ramafi GJ, Feldman C, Grimmer H, Visser SS, Anderson R (2004) Effects of platinum and palladium ions on the production and reactivity of neutrophil-derived reactive oxygen species. Free Radic Biol Med 36:1408–1417

    CAS  Google Scholar 

  • Turner N, Armitage M, Butler R, Ireland G (2004) An in vitro model to evaluate cell adhesion to metals used in implantation shows significant differences between palladium and gold or platinum. Cell Biol Int 28:541–547

    CAS  Google Scholar 

  • Vandooren J, Berghmans N, Dillen C, Van Aelst I, Ronsse I, Israel LL, Rosenberger I, Kreuter J, Lellouche JP, Michaeli S, Locatelli E, Franchini MC, Aiertza MK, Sanchez-Abella L, Loinaz I, Edwards DR, Shenkman L, Opdenakker G (2013) Intradermal air pouch leukocytosis as an in vivo test for nanoparticles. Int J Nanomedicine 8:4745

    Google Scholar 

  • Wilkinson KE, Palmberg L, Witasp E, Kupczyk M, Feliu N, Gerde P, Seisenbaeva GA, Fadeel B, Dahlen SE, Kessler VG (2011) Solution-engineered palladium nanoparticles: model for health effect studies of automotive particulate pollution. ACS Nano 5:5312–5324

    CAS  Google Scholar 

  • Yuan X, Nie W, He Z, Yang J, Shao B, Ma X, Zhang X, Bi Z, Sun L, Liang X, Tie Y, Liu Y, Mo F, Xie D, Wei Y, Wei X (2020) Carbon black nanoparticles induce cell necrosis through lysosomal membrane permeabilization and cause subsequent inflammatory response. Theranostics 10:4589–4605

    CAS  Google Scholar 

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Funding

The study was supported by grants from the Institut de recherche Robert-Sauvé en santé et en sécurité du travail (IRSST).

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  1. Laboratoire de recherche en inflammation et physiologie des granulocytes, Université du Québec, Institut National de la Recherche Scientifique (INRS), Centre Armand-Frappier Santé Biotechnologie, 531 boul. des Prairies, Laval, QC, H7V 1B7, Canada

    Pierrette Kwemo, Abdelaziz Saafane, Marion Vanharen, Isabelle Durocher & Denis Girard

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  1. Pierrette Kwemo
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  2. Abdelaziz Saafane
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  4. Isabelle Durocher
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Correspondence to Denis Girard.

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Kwemo, P., Saafane, A., Vanharen, M. et al. Impact of palladium nanoparticles (Pd-NPs) on the biology of neutrophils in vitro and on leukocyte attraction in vivo. J Nanopart Res 22, 350 (2020). https://doi.org/10.1007/s11051-020-05079-z

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